Social buffering in a bird

doi:10.1016/j.anbehav.2015.04.007

Animal Behaviour

Volume 105, July 2015, Pages 11-19

https://doi.org/10.1016/j.anbehav.2015.04.007 Get rights and content

Highlights

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We compared stress responses of chicks in the presence and absence of their mother.
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We also measured the hens' socially mediated arousal (SMA) during chick stress.
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The presence of the chicks' mother reduced chick behavioural response to stress.
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Mother hens are therefore able to buffer their chicks' stress response.
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Hens' SMA was negatively correlated with their effectiveness as a social buffer.

The presence of a conspecific can ameliorate an individual's stress response. This social buffering is known to be widespread in social mammals but the capacity of birds to act as social buffers has not yet been determined. We previously demonstrated that domestic hens, Gallus gallus domesticus, show socially mediated arousal when watching their chicks receiving an aversive air puff. Furthermore, the hens' expectation of the situation strongly influenced the chicks' behaviour. Here we examined whether hens act as a social buffer; reducing their chicks' stress response to an aversive stimulus. Pairs of chicks were exposed to an air puff treatment and a control, each with and without their mothers. Chicks showed a suite of responses to the air puff (including increased standing, reduced eye temperature, preening and ground pecking). Maternal absence exacerbated the chicks' preening and ground-pecking responses to this stressor. Individual hens varied in their effectiveness as a social buffer and this was associated with their socially mediated arousal when (matched pairs of) their chicks received an air puff. Specifically, the hens' heart rate increase was strongly negatively correlated with the degree to which chick preening and ground pecking increased with maternal presence. This is the first demonstration that avian mothers are able to reduce their chicks' stress responses to an aversive stimulus.

Section snippets

Ethical Note

This project was carried out following ethical approval by the University of Bristol (University Investigation Number: UB/07/002) and in accordance with the ASAB Guidelines for the Treatment of Animals in Behavioural Research and Teaching. At the end of the study all animals were rehomed to responsible smallholders.

Animals and Housing

Twelve broody hens (Indian game, N = 5, or Indian game crossed with Australorp, N = 7), aged 50–100 weeks, were obtained from a breeder and housed individually in a floor pen (1.5 × 1

Phase 1a: Response of Hens

As in our previous work (Edgar et al., 2011), we found a pronounced set of behavioural and physiological changes in hens when their chicks were subjected to an air puff. Hens had an increased heart rate (pretreatment period mean = 275 ± 14 bpm; treatment period mean = 337 ± 14 bpm; Wilks's lambda = 2.64, F_1,11 = 30.625, P < 0.001, partial eta² = 0.736), time spent standing alert (pretreatment period median = 19.9%, interquartile range, IQR = 82.6; treatment period median = 78.7%, IQR = 48.8; Wilks's lambda = 0.598, F_1,11 =

Discussion

Having previously demonstrated that chicks respond behaviourally to their mother's expectation of an aversive stimulus (Edgar, Paul, et al., 2013), our aim here was to investigate whether hens are able to buffer their chicks' stress response. Second, we sought to determine the extent of individual variation in the hen's responsiveness to chick stress and how this affects her social-buffering capacity.

Our previous studies identified an air puff as an aversive stimulus for chicks (Edgar, 2012)

Acknowledgments

This project was funded by the BBSRC (BB/J021679/1). We thank the two anonymous referees for their comments which helped to improve the manuscript.

References (51)

B. Apfelbeck et al.
Behavioural and hormonal effects of social isolation and neophobia in a gregarious bird species, the European starling (Sturnus vulgaris)
Hormones and Behaviour
(2008)
S.B. Banerjee et al.
Effect of isolation and conspecific presence in a novel environment on corticosterone concentrations in a social avian species, the zebra finch (Taeniopygia guttata)
Hormones and Behaviour
(2011)
G. Bermant
Intensity and rate of distress calling in chicks as a function of social contact
Animal Behaviour
(1963)
C. Busnardo et al.
Paraventricular nucleus modulates autonomic and neuroendocrine responses to acute restraint stress in rats
Autonomic Neuroscience
(2010)
J.L. Edgar et al.
Measuring empathic responses in animals
Applied Animal Behaviour Science
(2012)
J.L. Edgar et al.
Surface temperature changes in response to handling in domestic chickens
Physiology and Behaviour
(2013)
J.L. Edgar et al.
Protective mother hens: cognitive influences on the avian maternal response
Animal Behaviour
(2013)
M.W. Feltenstein et al.
Corticosterone responses in the chick social separation–stress paradigm
Physiology and Behaviour
(2003)
N.A. Geverink et al.
Responses of slaughter pigs to transport and lairage sounds
Physiology and Behaviour
(1998)
M. Gonzalez et al.
The effect of social buffering on fear responses in sheep (Ovis aries)
Applied Animal Behaviour Science
(2013)

D.A. Guzman et al.

Social reinstatement responses of meat-type chickens to familiar and unfamiliar conspecifics after exposure to an acute stressor

Applied Animal Behaviour Science

(2008)

M.B. Hennessy et al.

Social influences on cortisol and behavioral responses of preweaning, periadolescent, and adult guinea pigs

Physiology and Behaviour

(2002)

T.E. Hodges et al.

Effects of social context on endocrine function and Zif268 expression in response to an acute stressor in adolescent and adult rats

International Journal of Developmental Neuroscience

(2014)

C.M. Hostetler et al.

Social partners prevent alcohol relapse behavior in prairie voles

Psychoneuroendocrinology

(2014)

M.K. Hughes et al.

Frequency and intensity of chick distress calls: effects on maternal foodcalling in chickens

Behavioural Processes

(1982)

R.B. Jones et al.

Responses of pair-housed male and female domestic chicks to the removal of a companion

Applied Animal Behaviour Science

(1992)

E. Kanitz et al.

Social support attenuates the adverse consequences of social deprivation stress in domestic piglets

Hormones and Behaviour

(2014)

I.C. Kaufman et al.

Factors influencing distress calling in chicks, with special reference to temperature changes and social isolation

Animal Behaviour

(1961)

Y. Kiyokawa et al.

Social buffering reduces male rats' behavioral and corticosterone responses to a conditioned stimulus

Hormones and Behaviour

(2014)

Y. Kiyokawa et al.

A familiar conspecific is more effective than an unfamiliar conspecific for social buffering of conditioned fear responses in male rats

Behavioural Brain Research

(2014)

J.C. Lowe et al.

A novel telemetric logging system for recording physiological signals in unrestrained animals

Computers and Electronics in Agriculture

(2007)

R.H. Marin et al.

Effects of an acute stressor on fear and on the social reinstatement responses of domestic chicks to cagemates and strangers

Applied Animal Behaviour Science

(2001)

B.C. Mommer et al.

A test of maternal programming of offspring stress response to predation risk in threespine sticklebacks

Physiology and Behaviour

(2013)

C.J. Nicol et al.

Associations between welfare indicators and environmental choice in laying hens

Animal Behaviour

(2009)

F. Pittet et al.

Maternal styles in a precocial bird

Animal Behaviour

(2014)

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Citation Excerpt :
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View full text

Social buffering in a bird

Highlights

Section snippets

Ethical Note

Animals and Housing

Phase 1a: Response of Hens

Discussion

Acknowledgments

Hormones and Behaviour

Hormones and Behaviour

Animal Behaviour

Autonomic Neuroscience

Applied Animal Behaviour Science

Physiology and Behaviour

Animal Behaviour

Physiology and Behaviour

Physiology and Behaviour

Applied Animal Behaviour Science

Applied Animal Behaviour Science

Physiology and Behaviour

International Journal of Developmental Neuroscience

Psychoneuroendocrinology

Behavioural Processes

Applied Animal Behaviour Science

Hormones and Behaviour

Animal Behaviour

Hormones and Behaviour

Behavioural Brain Research

Computers and Electronics in Agriculture

Applied Animal Behaviour Science

Physiology and Behaviour

Animal Behaviour

Animal Behaviour